VEGFR-3 Neutralization Inhibits Ovarian Lymphangiogenesis, Follicle Maturation, and Murine Pregnancy
Identifieur interne : 002B67 ( Pmc/Corpus ); précédent : 002B66; suivant : 002B68VEGFR-3 Neutralization Inhibits Ovarian Lymphangiogenesis, Follicle Maturation, and Murine Pregnancy
Auteurs : Joseph M. Rutkowski ; Jong Eun Ihm ; Seung Tae Lee ; Witold W. Kilarski ; Veronique I. Greenwood ; Miriella C. Pasquier ; Alexandra Quazzola ; Didier Trono ; Jeffrey A. Hubbell ; Melody A. SwartzSource :
- The American Journal of Pathology [ 0002-9440 ] ; 2013.
Abstract
Lymphatic vessels surround follicles within the ovary, but their roles in folliculogenesis and pregnancy, as well as the necessity of lymphangiogenesis in follicle maturation and health, are undefined. We used systemic delivery of mF4-31C1, a specific antagonist vascular endothelial growth factor receptor 3 (VEGFR-3) antibody to block lymphangiogenesis in mice. VEGFR-3 neutralization for 2 weeks before mating blocked ovarian lymphangiogenesis at all stages of follicle maturation, most notably around corpora lutea, without significantly affecting follicular blood angiogenesis. The numbers of oocytes ovulated, fertilized, and implanted in the uterus were normal in these mice; however, pregnancies were unsuccessful because of retarded fetal growth and miscarriage. Fewer patent secondary follicles were isolated from treated ovaries, and isolated blastocysts exhibited reduced cell densities. Embryos from VEGFR-3–neutralized dams developed normally when transferred to untreated surrogates. Conversely, normal embryos transferred into mF4-31C1–treated dams led to the same fetal deficiencies observed with
Url:
DOI: 10.1016/j.ajpath.2013.07.031
PubMed: 24036251
PubMed Central: 3814520
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PMC:3814520Le document en format XML
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<author><name sortKey="Rutkowski, Joseph M" sort="Rutkowski, Joseph M" uniqKey="Rutkowski J" first="Joseph M." last="Rutkowski">Joseph M. Rutkowski</name>
<affiliation><nlm:aff id="aff1">Institute of Bioengineering, Swiss Federal Institute of Technology in Lausanne (EPFL), Lausanne, Switzerland</nlm:aff>
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<author><name sortKey="Ihm, Jong Eun" sort="Ihm, Jong Eun" uniqKey="Ihm J" first="Jong Eun" last="Ihm">Jong Eun Ihm</name>
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<author><name sortKey="Lee, Seung Tae" sort="Lee, Seung Tae" uniqKey="Lee S" first="Seung Tae" last="Lee">Seung Tae Lee</name>
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<author><name sortKey="Kilarski, Witold W" sort="Kilarski, Witold W" uniqKey="Kilarski W" first="Witold W." last="Kilarski">Witold W. Kilarski</name>
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<author><name sortKey="Greenwood, Veronique I" sort="Greenwood, Veronique I" uniqKey="Greenwood V" first="Veronique I." last="Greenwood">Veronique I. Greenwood</name>
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<author><name sortKey="Pasquier, Miriella C" sort="Pasquier, Miriella C" uniqKey="Pasquier M" first="Miriella C." last="Pasquier">Miriella C. Pasquier</name>
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<author><name sortKey="Quazzola, Alexandra" sort="Quazzola, Alexandra" uniqKey="Quazzola A" first="Alexandra" last="Quazzola">Alexandra Quazzola</name>
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<author><name sortKey="Swartz, Melody A" sort="Swartz, Melody A" uniqKey="Swartz M" first="Melody A." last="Swartz">Melody A. Swartz</name>
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<author><name sortKey="Ihm, Jong Eun" sort="Ihm, Jong Eun" uniqKey="Ihm J" first="Jong Eun" last="Ihm">Jong Eun Ihm</name>
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<author><name sortKey="Lee, Seung Tae" sort="Lee, Seung Tae" uniqKey="Lee S" first="Seung Tae" last="Lee">Seung Tae Lee</name>
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<author><name sortKey="Kilarski, Witold W" sort="Kilarski, Witold W" uniqKey="Kilarski W" first="Witold W." last="Kilarski">Witold W. Kilarski</name>
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<author><name sortKey="Greenwood, Veronique I" sort="Greenwood, Veronique I" uniqKey="Greenwood V" first="Veronique I." last="Greenwood">Veronique I. Greenwood</name>
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<author><name sortKey="Pasquier, Miriella C" sort="Pasquier, Miriella C" uniqKey="Pasquier M" first="Miriella C." last="Pasquier">Miriella C. Pasquier</name>
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<author><name sortKey="Quazzola, Alexandra" sort="Quazzola, Alexandra" uniqKey="Quazzola A" first="Alexandra" last="Quazzola">Alexandra Quazzola</name>
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<author><name sortKey="Swartz, Melody A" sort="Swartz, Melody A" uniqKey="Swartz M" first="Melody A." last="Swartz">Melody A. Swartz</name>
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<series><title level="j">The American Journal of Pathology</title>
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<front><div type="abstract" xml:lang="en"><p>Lymphatic vessels surround follicles within the ovary, but their roles in folliculogenesis and pregnancy, as well as the necessity of lymphangiogenesis in follicle maturation and health, are undefined. We used systemic delivery of mF4-31C1, a specific antagonist vascular endothelial growth factor receptor 3 (VEGFR-3) antibody to block lymphangiogenesis in mice. VEGFR-3 neutralization for 2 weeks before mating blocked ovarian lymphangiogenesis at all stages of follicle maturation, most notably around corpora lutea, without significantly affecting follicular blood angiogenesis. The numbers of oocytes ovulated, fertilized, and implanted in the uterus were normal in these mice; however, pregnancies were unsuccessful because of retarded fetal growth and miscarriage. Fewer patent secondary follicles were isolated from treated ovaries, and isolated blastocysts exhibited reduced cell densities. Embryos from VEGFR-3–neutralized dams developed normally when transferred to untreated surrogates. Conversely, normal embryos transferred into mF4-31C1–treated dams led to the same fetal deficiencies observed with <italic>in situ</italic>
gestation. Although no significant changes were measured in uterine blood or lymphatic vascular densities, VEGFR-3 neutralization reduced serum and ovarian estradiol concentrations during gestation. VEGFR-3–mediated lymphangiogenesis thus appears to modulate the folliculogenic microenvironment and may be necessary for maintenance of hormone levels during pregnancy; both of these are novel roles for the lymphatic vasculature.</p>
</div>
</front>
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<front><journal-meta><journal-id journal-id-type="nlm-ta">Am J Pathol</journal-id>
<journal-id journal-id-type="iso-abbrev">Am. J. Pathol</journal-id>
<journal-title-group><journal-title>The American Journal of Pathology</journal-title>
</journal-title-group>
<issn pub-type="ppub">0002-9440</issn>
<issn pub-type="epub">1525-2191</issn>
<publisher><publisher-name>American Society for Investigative Pathology</publisher-name>
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<article-meta><article-id pub-id-type="pmid">24036251</article-id>
<article-id pub-id-type="pmc">3814520</article-id>
<article-id pub-id-type="publisher-id">S0002-9440(13)00555-5</article-id>
<article-id pub-id-type="doi">10.1016/j.ajpath.2013.07.031</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Regular Article</subject>
<subj-group><subject>Metabolic, Endocrine, and Genitourinary Pathobiology</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>VEGFR-3 Neutralization Inhibits Ovarian Lymphangiogenesis, Follicle Maturation, and Murine Pregnancy</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Rutkowski</surname>
<given-names>Joseph M.</given-names>
</name>
<xref rid="aff1" ref-type="aff">∗</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ihm</surname>
<given-names>Jong Eun</given-names>
</name>
<xref rid="aff1" ref-type="aff">∗</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Lee</surname>
<given-names>Seung Tae</given-names>
</name>
<xref rid="aff1" ref-type="aff">∗</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Kilarski</surname>
<given-names>Witold W.</given-names>
</name>
<xref rid="aff1" ref-type="aff">∗</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Greenwood</surname>
<given-names>Veronique I.</given-names>
</name>
<xref rid="aff1" ref-type="aff">∗</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Pasquier</surname>
<given-names>Miriella C.</given-names>
</name>
<xref rid="aff1" ref-type="aff">∗</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Quazzola</surname>
<given-names>Alexandra</given-names>
</name>
<xref rid="aff2" ref-type="aff">†</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Trono</surname>
<given-names>Didier</given-names>
</name>
<xref rid="aff2" ref-type="aff">†</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Hubbell</surname>
<given-names>Jeffrey A.</given-names>
</name>
<xref rid="aff1" ref-type="aff">∗</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Swartz</surname>
<given-names>Melody A.</given-names>
</name>
<email>melody.swartz@epfl.ch</email>
<xref rid="aff1" ref-type="aff">∗</xref>
<xref rid="cor1" ref-type="corresp">∗</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>∗</label>
Institute of Bioengineering, Swiss Federal Institute of Technology in Lausanne (EPFL), Lausanne, Switzerland</aff>
<aff id="aff2"><label>†</label>
Global Health Institute, Swiss Federal Institute of Technology in Lausanne (EPFL), Lausanne, Switzerland</aff>
<author-notes><corresp id="cor1"><label>∗</label>
Address correspondence to Melody A. Swartz, Ph.D., Institute of Bioengineering, School of Life Sciences, Laboratory of Lymphatic and Cancer Bioengineering (LLCB), Station 15, École Polytechnique Fédérale de Lausanne (EPFL), 1015 Lausanne, Switzerland. <email>melody.swartz@epfl.ch</email>
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<pub-date pub-type="pmc-release"><day>1</day>
<month>11</month>
<year>2014</year>
</pub-date>
<pmc-comment> PMC Release delay is 12 months and 0 days and was based on .</pmc-comment>
<pub-date pub-type="ppub"><month>11</month>
<year>2013</year>
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<volume>183</volume>
<issue>5</issue>
<fpage>1596</fpage>
<lpage>1607</lpage>
<history><date date-type="accepted"><day>31</day>
<month>7</month>
<year>2013</year>
</date>
</history>
<permissions><copyright-statement>© 2013 American Society for Investigative Pathology. Published by Elsevier Inc. All rights reserved.</copyright-statement>
<copyright-year>2013</copyright-year>
<copyright-holder>American Society for Investigative Pathology</copyright-holder>
<license><license-p>This document may be redistributed and reused, subject to <ext-link ext-link-type="uri" xlink:href="http://www.elsevier.com/wps/find/authorsview.authors/supplementalterms1.0">certain conditions</ext-link>
.</license-p>
</license>
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<abstract><p>Lymphatic vessels surround follicles within the ovary, but their roles in folliculogenesis and pregnancy, as well as the necessity of lymphangiogenesis in follicle maturation and health, are undefined. We used systemic delivery of mF4-31C1, a specific antagonist vascular endothelial growth factor receptor 3 (VEGFR-3) antibody to block lymphangiogenesis in mice. VEGFR-3 neutralization for 2 weeks before mating blocked ovarian lymphangiogenesis at all stages of follicle maturation, most notably around corpora lutea, without significantly affecting follicular blood angiogenesis. The numbers of oocytes ovulated, fertilized, and implanted in the uterus were normal in these mice; however, pregnancies were unsuccessful because of retarded fetal growth and miscarriage. Fewer patent secondary follicles were isolated from treated ovaries, and isolated blastocysts exhibited reduced cell densities. Embryos from VEGFR-3–neutralized dams developed normally when transferred to untreated surrogates. Conversely, normal embryos transferred into mF4-31C1–treated dams led to the same fetal deficiencies observed with <italic>in situ</italic>
gestation. Although no significant changes were measured in uterine blood or lymphatic vascular densities, VEGFR-3 neutralization reduced serum and ovarian estradiol concentrations during gestation. VEGFR-3–mediated lymphangiogenesis thus appears to modulate the folliculogenic microenvironment and may be necessary for maintenance of hormone levels during pregnancy; both of these are novel roles for the lymphatic vasculature.</p>
</abstract>
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</front>
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